Molecular reconstitution of functional GABAergic synapses with expression of neuroligin-2 and GABAA receptors

Molecular and Cellular Neuroscience

Volumn 35, Issue 1, 2007, Pages 14-23

  Dong, Ning ^a   Qi, Jinshun ^a,b   Chen, Gong ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b SHANXI MEDICAL UNIVERSITY   (China)

Author keywords

GABAA receptor; GABAergic synapse; Neuroligin; Postsynaptic; Presynaptic; Synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANTIBODY; NEUROLIGIN; NEUROLIGIN 1; NEUROLIGIN 2; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; GABAERGIC SYSTEM; HUMAN; HUMAN CELL; HYPOTHALAMUS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPSE;

ANIMALS; CELLS, CULTURED; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; HUMANS; HYPOTHALAMUS, MIDDLE; INHIBITORY POSTSYNAPTIC POTENTIALS; KIDNEY; KINETICS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; TRANSFECTION;

EID: 34247341381     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.01.013     Document Type: Article

References (58)

1. Alldred M.J., Mulder-Rosi J., Lingenfelter S.E., Chen G., and Luscher B. Distinct gamma2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin. J. Neurosci. 25 (2005) 594-603
2. Ango F., di Cristo G., Higashiyama H., Bennett V., Wu P., and Huang Z.J. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119 (2004) 257-272
3. Benson D.L., and Tanaka H. N-cadherin redistribution during synaptogenesis in hippocampal neurons. J. Neurosci. 18 (1998) 6892-6904
4. Betz W.J., and Bewick G.S. Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255 (1992) 200-203
5. Biederer T., and Sudhof T.C. Mints as adaptors. Direct binding to neurexins and recruitment of munc18. J. Biol. Chem. 275 (2000) 39803-39806
6. Biederer T., Sara Y., Mozhayeva M., Atasoy D., Liu X., Kavalali E.T., and Sudhof T.C. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297 (2002) 1525-1531
7. Boucard A.A., Chubykin A.A., Comoletti D., Taylor P., and Sudhof T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 48 (2005) 229-236
8. Bozdagi O., Valcin M., Poskanzer K., Tanaka H., and Benson D.L. Temporally distinct demands for classic cadherins in synapse formation and maturation. Mol. Cell. Neurosci. 27 (2004) 509-521
9. Chavis P., and Westbrook G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411 (2001) 317-321
10. Chen G., Trombley P.Q., and van den Pol A.N. GABA receptors precede glutamate receptors in hypothalamic development; differential regulation by astrocytes. J. Neurophysiol. 74 (1995) 1473-1484
11. Chen G., Trombley P.Q., and van den Pol A.N. Excitatory actions of GABA in developing rat hypothalamic neurones. J. Physiol. 494 (1996) 451-464
12. Chen Y., Deng L.B., Maeno-Hikichi Y., Lai M.Z., Chang S.H., Chen G., and Zhang J.F. Formation of an endophilin-Ca2+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis. Cell 115 (2003) 37-48
13. Chen G., Harata N., and Tsien R.W. Paired-pulse depression of unitary quantal amplitude at single hippocampal synapses. Proc. Natl. Acad. Sci. 101 (2004) 1063-1068
14. Chih B., Engelman H., and Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307 (2005) 1324-1328
15. Chih B., Gollan L., and Scheiffele P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51 (2006) 171-178
16. Craig A.M., Graf E.R., and Linhoff M.W. How to build a central synapse: clues from cell culture. Trends Neurosci. 29 (2006) 8-20
17. Dean C., Scholl F.G., Choih J., DeMaria S., Berger J., Isacoff E., and Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6 (2003) 708-716
18. Decavel C., and Van den Pol A.N. GABA: a dominant neurotransmitter in the hypothalamus. J. Comp. Neurol. 302 (1990) 1019-1037
19. Dumoulin A., Levi S., Riveau B., Gasnier B., and Triller A. Formation of mixed glycine and GABAergic synapses in cultured spinal cord neurons. Eur. J. Neurosci. 12 (2000) 3883-3892
20. Essrich C., Lorez M., Benson J.A., Fritschy J.M., and Luscher B. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat.Neurosci. 1 (1998) 563-571
21. Fritschy J.M., and Brunig I. Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol. Ther. 98 (2003) 299-323
22. Fu Z., Washbourne P., Ortinski P., and Vicini S. Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors. J. Neurophysiol. 90 (2003) 3950-3957
23. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., and Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119 (2004) 1013-1026
24. Graf E.R., Kang Y., Hauner A.M., and Craig A.M. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J. Neurosci. 26 (2006) 4256-4265
25. Hata Y., Butz S., and Sudhof T.C. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16 (1996) 2488-2494
26. Ichtchenko K., Hata Y., Nguyen T., Ullrich B., Missler M., Moomaw C., and Sudhof T.C. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 81 (1995) 435-443
27. Ichtchenko K., Nguyen T., and Sudhof T.C. Structures, alternative splicing, and neurexin binding of multiple neuroligins. J. Biol. Chem. 271 (1996) 2676-2682
28. Irie M., Hata Y., Takeuchi M., Ichtchenko K., Toyoda A., Hirao K., Takai Y., Rosahl T.W., and Sudhof T.C. Binding of neuroligins to PSD-95. Science 277 (1997) 1511-1515
29. Jiang M., and Chen G. High Ca2+-phosphate transfection efficiency in low-density neuronal cultures. Nat. Protocols 1 (2006) 695-700
30. Jones M.V., and Westbrook G.L. Desensitized states prolong GABAA channel responses to brief agonist pulses. Neuron 15 (1995) 181-191
31. Kay A.R., Alfonso A., Alford S., Cline H.T., Holgado A.M., Sakmann B., Snitsarev V.A., Stricker T.P., Takahashi M., and Wu L.G. Imaging synaptic activity in intact brain and slices with FM1-43 in C. elegans, lamprey, and rat. Neuron 24 (1999) 809-817
32. Kayser M.S., McClelland A.C., Hughes E.G., and Dalva M.B. Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J. Neurosci. 26 (2006) 12152-12164
33. Kim E., and Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5 (2004) 771-781
34. Kim S., Burette A., Chung H.S., Kwon S.K., Woo J., Lee H.W., Kim K., Kim H., Weinberg R.J., and Kim E. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat. Neurosci. 9 (2006) 1294-1301
35. Levi S., Logan S.M., Tovar K.R., and Craig A.M. Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J. Neurosci. 24 (2004) 207-217
36. Levinson J.N., and El-Husseini A. New players tip the scales in the balance between excitatory and inhibitory synapses. Mol. Pain 1 (2005) 12
37. Levinson J.N., Chery N., Huang K., Wong T.P., Gerrow K., Kang R., Prange O., Wang Y.T., and El-Husseini A. Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity. J. Biol. Chem. 280 (2005) 17312-17319
38. Lise M.F., and El-Husseini A. The neuroligin and neurexin families: from structure to function at the synapse. Cell. Mol. Life Sci. 63 (2006) 1833-1849
39. Luscher B., and Keller C.A. Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol. Ther. 102 (2004) 194-220
40. Missler M., Zhang W., Rohlmann A., Kattenstroth G., Hammer R.E., Gottmann K., and Sudhof T.C. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423 (2003) 939-948
41. Moss S.J., and Smart T.G. Constructing inhibitory synapses. Nat. Rev., Neurosci. 2 (2001) 240-250
42. Nam C.I., and Chen L. Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 6137-6142
43. Nguyen T., and Sudhof T.C. Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J. Biol. Chem. 272 (1997) 26032-26039
44. Prange O., Wong T.P., Gerrow K., Wang Y.T., and El-Husseini A. A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 13915-13920
45. Ryan T.A., Reuter H., Wendland B., Schweizer F.E., Tsien R.W., and Smith S.J. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11 (1993) 713-724
46. Sara Y., Biederer T., Atasoy D., Chubykin A., Mozhayeva M.G., Sudhof T.C., and Kavalali E.T. Selective capability of SynCAM and neuroligin for functional synapse assembly. J. Neurosci. 25 (2005) 260-270
47. Sassoe-Pognetto M., and Fritschy J.M. Mini-review: gephyrin, a major postsynaptic protein of GABAergic synapses. Eur. J. Neurosci. 12 (2000) 2205-2210
48. Sassoe-Pognetto M., Kirsch J., Grunert U., Greferath U., Fritschy J.M., Mohler H., Betz H., and Wassle H. Colocalization of gephyrin and GABAA-receptor subunits in the rat retina. J. Comp. Neurol. 357 (1995) 1-14
49. Scheiffele P., Fan J., Choih J., Fetter R., and Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101 (2000) 657-669
50. Song J.Y., Ichtchenko K., Sudhof T.C., and Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 1100-1105
51. Studler B., Sidler C., and Fritschy J.M. Differential regulation of GABA(A) receptor and gephyrin postsynaptic clustering in immature hippocampal neuronal cultures. J. Comp. Neurol. 484 (2005) 344-355
52. Sumita K., Sato Y., Iida J., Kawata A., Hamano M., Hirabayashi S., Ohno K., Peles E., and Hata Y. Synaptic scaffolding molecule (S-SCAM) membrane-associated guanylate kinase with inverted organization (MAGI)-2 is associated with cell adhesion molecules at inhibitory synapses in rat hippocampal neurons. J. Neurochem. (2006)
53. Ullrich B., Ushkaryov Y.A., and Sudhof T.C. Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron 14 (1995) 497-507
54. Ushkaryov Y.A., Petrenko A.G., Geppert M., and Sudhof T.C. Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science 257 (1992) 50-56
55. van Rijnsoever C., Sidler C., and Fritschy J.M. Internalized GABA-receptor subunits are transferred to an intracellular pool associated with the postsynaptic density. Eur. J. Neurosci. 21 (2005) 327-338
56. Varoqueaux F., Jamain S., and Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 83 (2004) 449-456
57. Varoqueaux F., Aramuni G., Rawson R.L., Mohrmann R., Missler M., Gottmann K., Zhang W., Sudhof T.C., and Brose N. Neuroligins determine synapse maturation and function. Neuron 51 (2006) 741-754
58. Yao J., Qi J., and Chen G. Actin-dependent activation of presynaptic silent synapses contributes to long-term synaptic plasticity in developing hippocampal neurons. J. Neurosci. 26 (2006) 8137-8147